Skip to main content

Advertisement

Log in

The roles of ascorbic acid and glutathione in symptom alleviation to SA-deficient plants infected with RNA viruses

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Salicylic acid (SA) is required for plant systemic acquired resistance (SAR) to viruses. However, SA-deficient plants adapt to RNA virus infections better, which show a lighter symptom and have less reactive oxygen species (ROS) accumulation. The virus replication levels are higher in the SA-deficient plants during the first 10 days, but lower than the wild-type seedlings after 20 dpi. The higher level of glutathione and ascorbic acid (AsA) in SA-deficient plants may contribute to their alleviated symptoms. Solo virus-control method for mortal viruses results in necrosis and chlorosis, no matter what level of virus RNAs would accumulate. Contrastingly, early and high-dose AsA treatment alleviates the symptom, and eventually inhibits virus replication after 20 days. ROS eliminators could not imitate the effect of AsA, and could neither alleviate symptom nor inhibit virus replication. It suggests that both symptom alleviation and virus replication control should be considered for plant virus cures.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

AsA:

Ascorbic acid

CMV:

Cucumber mosaic virus

CPZ:

Chlorpromazine

DMTU:

Dimethylthiourea

dpi:

Days after inoculation

HR:

Hypersensitive response

JA:

Jasmonic acid

OTC:

l-2-Oxothiazolidine-4-carboxylic acid

ROS:

Reactive oxygen species

SA:

Salicylic acid

SAR:

Systemic acquired resistance

TCV:

Turnip crinkle virus

TNV:

Tobacco necrosis virus

References

  • Abreu ME, Munné-Bosch S (2009) Salicylic acid deficiency in NahG transgenic lines and sid2 mutants increases seed yield in the annual plant Arabidopsis thaliana. J Exp Bot 60:1261–1271

    Article  PubMed  CAS  Google Scholar 

  • Barth C, Moeder W, Klessig DF, Conklin PL (2004) The timing of senescence and response to pathogens is altered in the ascorbate-deficient Arabidopsis mutant vitamin c-1. Plant Physiol 134:1784–1792

    Article  PubMed  CAS  Google Scholar 

  • Borsani O, Valpuesta V, Botella MA (2001) Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol 126:1024–1030

    Article  PubMed  CAS  Google Scholar 

  • Cao Y, Zhang ZW, Xue LW, Du JB, Shang J, Xu F, Yuan S, Lin HH (2009) Lack of salicylic acid in NahG Arabidopsis protects plants against moderate salt stress. Z Naturforsch 64c:231–238

    Google Scholar 

  • Chaturvedi R, Shah J (2007) Salicylic acid in plant disease resistance. In: Hayat S, Ahmad A (eds) Salicylic acid—a plant hormone. Springer, Dordrecht, pp 335–370

    Chapter  Google Scholar 

  • Colville L, Smirnoff N (2008) Antioxidant status, peroxidase activity, and PR protein transcript levels in ascorbate-deficient Arabidopsis thaliana vtc mutants. J Exp Bot 59:3857–3868

    Article  PubMed  CAS  Google Scholar 

  • Delaney TP, Uknes S, Vernooij B, Friedrich L, Weymann K, Negrotto D, Gaffney T, Gut-Rella M, Kessmann H, Ward E, Ryals J (1994) A central role of salicylic acid in plant disease resistance. Science 266:1247–1250

    Article  PubMed  CAS  Google Scholar 

  • Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209

    Article  PubMed  CAS  Google Scholar 

  • Foyer CH, Noctor G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071

    Article  CAS  Google Scholar 

  • Friedrich L, Vernooij B, Gaffney T, Morse A, Ryals J (1995) Characterization of tobacco plants expressing a bacterial salicylate hydroxylase gene. Plant Mol Biol 29:959–968

    Article  PubMed  CAS  Google Scholar 

  • Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S, Ward E, Kessmann H, Ryals J (1993) Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261:754–756

    Article  PubMed  CAS  Google Scholar 

  • He K, Gou XP, Yuan T, Lin HH, Asami T, Yoshida S, Russell SD, Li J (2007) BAK1 and BKK1 regulate brassinosteroid-dependent growth and brassinosteroid-independent cell-death pathways. Curr Biol 17:1109–1115

    Article  PubMed  CAS  Google Scholar 

  • Herschbach C, Scheerer U, Rennenberg H (2010) Redox states of glutathione and ascorbate in root tips of poplar (Populus tremula × P. alba) depend on phloem transport from the shoot to the roots. J Exp Bot 61:1065–1074

    Article  PubMed  CAS  Google Scholar 

  • Liu WJ, Chen YE, Tian WJ, Du JB, Zhang ZW, Xu F, Zhang F, Yuan S, Lin HH (2009) Dephosphorylation of photosystem II proteins and phosphorylation of CP29 in barley photosynthetic membranes as a response to water stress. Biochim Biophys Acta 1787:1238–1245

    Article  PubMed  CAS  Google Scholar 

  • Love AJ, Yun BW, Laval V, Loake GJ, Milner JJ (2005) Cauliflower mosaic virus, a compatible pathogen of Arabidopsis, engages three distinct defense-signaling pathways and activates rapid systemic generation of reactive oxygen species. Plant Physiol 139:935–948

    Article  PubMed  CAS  Google Scholar 

  • Luo MH, Yuan S, Chen YE, Liu WJ, Du JB, Lei T, Wang MB, Lin HH (2009) Effects of salicylic acid on the photosystem II of barley seedlings under osmotic stress. Biol Plant 53:663–669

    Article  CAS  Google Scholar 

  • Mukherjee M, Larrimore KE, Ahmed NJ, Bedick TS, Barghouthi NT, Traw MB, Barth C (2010) Ascorbic acid deficiency in Arabidopsis induces constitutive priming that is dependent on hydrogen peroxide, salicylic acid, and the NPR1 Gene. Mol Plant Microbe Interact 23:340–351

    Article  PubMed  CAS  Google Scholar 

  • Murphy AM, Gilliland A, York CJ, Hyman B, Carr JP (2004) High-level expression of alternative oxidase protein sequences enhances the spread of viral vectors in resistant and susceptible plants. J Gen Virol 85:3777–3786

    Article  PubMed  CAS  Google Scholar 

  • Nawrath C, Métraux JP (1999) Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell 11:1393–1404

    Article  PubMed  CAS  Google Scholar 

  • Nawrath C, Heck S, Parinthawong N, Métraux JP (2002) EDS5, an essential component of salicylic acid-dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family. Plant Cell 14:275–286

    Article  PubMed  CAS  Google Scholar 

  • Park SW, Kaimoyo E, Kumar D, Mosher S, Klessig DF (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318:113–116

    Article  PubMed  CAS  Google Scholar 

  • Pastori GM, Kiddle G, Antoniw J, Bernard S, Veljovic-Jovanovic S, Verrier PJ, Noctor G, Foyer CH (2003) Leaf vitamin C contents modulate plant defense transcripts and regulate genes that control development through hormone signaling. Plant Cell 15:939–951

    Article  PubMed  CAS  Google Scholar 

  • Pavet V, Olmos E, Kiddle G, Mowla S, Kumar S, Antoniw J, Alvarez ME, Foyer CH (2005) Ascorbic acid deficiency activates cell death and disease resistance responses in Arabidopsis. Plant Physiol 139:1291–1303

    Article  PubMed  CAS  Google Scholar 

  • Pignocchi C, Kiddle G, Hernandez I, Foster SJ, Asensi A, Taybi T, Barnes J, Foyer CH (2006) Ascorbate oxidase-dependent changes in the redox state of the apoplast modulate gene transcript accumulation leading to modified hormone signaling and orchestration of defense processes in tobacco. Plant Physiol 141:423–435

    Article  PubMed  CAS  Google Scholar 

  • Sasvari Z, Bach S, Blondel M, Nagy PD (2009) Inhibition of RNA recruitment and replication of an RNA virus by acridine derivatives with known anti-prion activities. PLoS ONE 4:e7376

    Article  PubMed  Google Scholar 

  • Scott IM, Clarke SM, Wood JE, Mur LAJ (2004) Salicylate accumulation inhibits growth at chilling temperature in Arabidopsis. Plant Physiol 135:1040–1049

    Article  PubMed  CAS  Google Scholar 

  • Shang J, Xi DH, Huang QR, Xu MY, Yuan S, Wang SD, Jia SD, Cao S, Zhou ZL, Lin HH (2009) Effect of two satellite RNAs on the Nicotiana glutinosa infected with Cucumber mosaic virus (CMV). Physiol Mol Plant Pathol 74:184–190

    Article  CAS  Google Scholar 

  • Shang J, Xi DH, Xu F, Wang SD, Cao S, Xu MY, Zhao PP, Wang JH, Jia SD, Zhang ZW, Yuan S, Lin HH (2011) A broad-spectrum, efficient and nontransgenic approach to control plant viruses by application of salicylic acid and jasmonic acid. Planta 233:299–308

    Article  PubMed  CAS  Google Scholar 

  • Smirnoff N (1996) The function and metabolism of ascorbic acid in plants. Ann Bot 78:661–669

    Article  CAS  Google Scholar 

  • Spoel SH, Koornneef A, Claessens SMC, Korzelius JP, Van-Pelt JA, Mueller MJ, Buchala AJ, Métraux JP, Brown R, Kazan K, Van-Loon LC, Dong XN, Pieterse CMJ (2003) NPR1 modulates cross-talk between salicylate-and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760–770

    Article  PubMed  CAS  Google Scholar 

  • Spoel SH, Mou Z, Tada Y, Spivey NW, Genschik P, Dong XN (2009) Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell 137:60–872

    Article  Google Scholar 

  • Sun X, Simon AE (2003) Fitness of a turnip crinkle virus satellite RNA correlates with a sequence-nonspecific hairpin and flanking sequences that enhance replication and repress the accumulation of virions. J Virol 77:880–7889

    Google Scholar 

  • Xu PZ, Yuan S, Li Y, Zhang HY, Wang XD, Lin HH, Wu XJ (2007) Genome-wide non-mendelian inheritance of genomic RNA cache in rice with high frequency. Genome 50:297–302

    Article  PubMed  CAS  Google Scholar 

  • Yang YN, Qi M, Mei CS (2004) Endogenous salicylic acid protects rice plants from oxidative damage caused by aging as well as biotic and abiotic stress. Plant J 40:909–919

    Article  PubMed  CAS  Google Scholar 

  • Yuan S, Lin HH (2008) Role of salicylic acid in plant abiotic stress. Z Naturforsch 63c:313–320

    Google Scholar 

  • Zechmann B, Zellnig G, Urbanek-Krajnc A, Müller M (2007) Artificial elevation of glutathione affects symptom development in ZYMV-infected Cucurbita pepo L. plants. Arch Virol 152:747–762

    Article  PubMed  CAS  Google Scholar 

  • Zhang A, Jiang M, Zhang J, Tan M, Hu X (2006) Mitogen-activated protein kinase is involved in abscisic acid-induced antioxidant defense and acts downstream of reactive oxygen species production in leaves of maize plants. Plant Physiol 141:475–487

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Arabidopsis thaliana seeds carrying NahG gene were gifts from Prof. Jia Li (University of Oklahoma, USA & Lanzhou University, China). We thank Mr. Rupu Xiao (Certcana Systems Institute, Ontario, Canada) for the language edition. This work was supported by National Nature Science Foundation of China (91017004, 31071669, 31070210, 30970214 and 30800071) and Sichuan Nature Science Foundation (2010JQ0080) and the National Key Basic Research ‘973’ Program of China (2009CB118500).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to De-Hui Xi or Hong-Hui Lin.

Additional information

S. -D. Wang, F. Zhu and S. Yuan contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 650 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, SD., Zhu, F., Yuan, S. et al. The roles of ascorbic acid and glutathione in symptom alleviation to SA-deficient plants infected with RNA viruses. Planta 234, 171–181 (2011). https://doi.org/10.1007/s00425-011-1391-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-011-1391-2

Keywords

Navigation